Novel scalable 3D cell based model for in vitro neurotoxicity testing: Combining human differentiated neurospheres with gene expression and functional endpoints

Journal of Biotechnology

Volumn 205, Issue , 2015, Pages 82-92

  Terrasso, Ana Paula ^a,b   Pinto, Catarina ^a,b   Serra, Margarida ^a,b   Filipe, Augusto ^c   Almeida, Susana ^c   Ferreira, Ana Lúcia ^c   Pedroso, Pedro ^c   Brito, Catarina ^a,b   Alves, Paula Marques ^a,b  

^a INSTITUTO DE BIOLOGIA EXPERIMENTAL E TECNOLÓGICA   (Portugal)

^b INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^c Tecnimede Group   (Portugal)

Author keywords

3D culture; Astrocyte; Human neurotoxicity; Neural differentiation; Neurospheres

Indexed keywords

CELLS; CYTOLOGY; GENES; NEURONS; TOXICITY;

3-D CULTURES; ASTROCYTE; NEURAL DIFFERENTIATIONS; NEUROSPHERES; NEUROTOXICITY;

GENE EXPRESSION;

ACRYLAMIDE; CHLORAMPHENICOL; PEROXIDE; TERT-BUTYL PEROXIDE;

ASTROCYTE; BIOLOGICAL MODEL; CELL CULTURE TECHNIQUE; CELL DIFFERENTIATION; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION; HUMAN; MULTICELLULAR SPHEROID; NERVE CELL; PROCEDURES; TOXICITY TESTING; TUMOR CELL LINE;

ACRYLAMIDE; ASTROCYTES; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINE, TUMOR; CHLORAMPHENICOL; GENE EXPRESSION; HUMANS; MODELS, BIOLOGICAL; NEURONS; PEROXIDES; SPHEROIDS, CELLULAR; TOXICITY TESTS;

EID: 84939934592     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2014.12.011     Document Type: Article

References (48)

1. Allen N.J., Barres B.A. Glia-more than just brain glue. Neuroscience 2009, 457:675-677.
2. Alonso-Nanclares L., Defelipe J. Vesicular glutamate transporter 1 immunostaining in the normal and epileptic human cerebral cortex. Neuroscience 2005, 134:59-68. 10.1016/j.neuroscience.2005.03.038.
3. Amaral A.I., Teixeira A.P., Håkonsen B.I., Sonnewald U., Alves P.M. A comprehensive metabolic profile of cultured astrocytes using isotopic transient metabolic flux analysis and C-labeled glucose. Front. Neuroenergetics 2011, 3(5). 10.3389/fnene.2011.00005.
4. Bani-Yaghoub M., Felker J.M., Naus C.C.G. Human NT2/D1 cells differentiate into functional astrocytes. Neuroreport 1999, 10:3843-3846. 10.1097/00001756-199912160-00022.
5. Barber D.S., LoPachin R.M. Proteomic analysis of acrylamide-protein adduct formation in rat brain synaptosomes. Toxicol. Appl. Pharmacol. 2004, 201:120-136. 10.1016/j.taap.2004.05.008.
6. Breier J.M., Gassmann K., Kayser R., Stegeman H., De Groot D., Fritsche E., Shafer T.J. Neural progenitor cells as models for high-throughput screens of developmental neurotoxicity: state of the science. Neurotoxicol. Teratol. 2010, 32:4-15. 10.1016/j.ntt.2009.06.005.
7. Breslin S., Driscoll L.O. Three-dimensional cell culture: the missing link in drug discovery. Drug Discov. Today 2013, 18:240-249.
8. Brito C., Escrevente C., Reis C.A., Lee V.M., Trojanowski J.Q., Costa J. Increased levels of fucosyltransferase IX and carbohydrate lewis X adhesion determinant in human NT2N neurons. J. Neurosci. Res. 2007, 1270:1260-1270. 10.1002/jnr.
9. Brito C., Simão D., Costa I., Malpique R., Pereira C.I., Fernandes P., Serra M., Schwarz S.C., Schwarz J., Kremer E.J., Alves P.M. Generation and genetic modification of 3D cultures of human dopaminergic neurons derived from neural progenitor cells. Methods 2012, 56:452-460.
10. Cantini G., Pisati F., Pessina S., Finocchiaro G., Pellegatta S. Immunotherapy against the radial glia marker GLAST ffectively triggeres specific antitumor effectors without autoimmunity. Oncoimmunology 2012, 1-10.
11. Chen Y., Swanson R.A. Astrocytes and Brain Injury 2003, 137-149. 10.1097/01.WCB.0000044631.80210.3C.
12. Conti L., Cattaneo E. Neural stem cell systems: physiological players or in vitro entities?. Nat. Rev. Neurosci. 2010, 11:176-187. 10.1038/nrn2761.
13. Donato R., Sorci G., Riuzzi F., Arcuri C., Bianchi R., Brozzi F., Tubaro C., Giambanco I. S100B's double life: intracellular regulator and extracellular signal. Biochim. Biophys. Acta 2009, 1793:1008-1022. 10.1016/j.bbamcr.2008.11.009.
14. Exon J.H. A review of the toxicology of acrylamide. J. Toxicol. Environ. Health. B. Crit. Rev. 2006, 9:397-412. 10.1080/10937400600681430.
15. Federico A., Cardaioli E., Da Pozzo P., Formichi P., Gallus G.N., Radi E. Mitochondria, oxidative stress and neurodegeneration. J. Neurol. Sci. 2012, 322:254-262. 10.1016/j.jns.2012.05.030.
16. Fennema E., Rivron N., Rouwkema J., van Blitterswijk C., de Boer J. Spheroid culture as a tool for creating 3D complex tissues. Trends Biotechnol. 2013, 31:108-115. 10.1016/j.tibtech.2012.12.003.
17. Gaffield M.a., Betz W.J. Imaging synaptic vesicle exocytosis and endocytosis with FM dyes. Nat. Protoc. 2006, 1:2916-2921. 10.1038/nprot.2006.476.
18. Gartlon J., Kinsner a, Bal-Price a, Coecke S., Clothier R.H. Evaluation of a proposed in vitro test strategy using neuronal and non-neuronal cell systems for detecting neurotoxicity. Toxicol. In Vitro 2006, 20:1569-1581. 10.1016/j.tiv.2006.07.009.
19. Goodfellow C.E., Graham S.E., Dragunow M., Glass M. Characterization of NTera2/D1 cells as a model system for the investigation of cannabinoid function in human neurons and astrocytes. J. Neurosci. Res. 2011, 89:1685-1697. 10.1002/jnr.22692.
20. Grill M.F., Maganti R.K. Neurotoxic effects associated with antibiotic use: management considerations. Br. J. Clin. Pharmacol. 2011, 72:381-393. 10.1111/j. 1365-2125.2011.03991.x.
21. Gupta K., Patani R., Baxter P., Serio A., Story D., Tsujita T., Hayes J.D., Pedersen R.A., Hardingham G.E., Chandran S. Human embryonic stem cell derived astrocytes mediate non-cell-autonomous neuroprotection through endogenous and drug-induced mechanisms. Cell Death Differ. 2012, 19:779-787. 10.1038/cdd.2011.154.
22. Hill E.J., Woehrling E.K., Prince M., Coleman M.D. Differentiating human NT2/D1 neurospheres as a versatile in vitro 3D model system for developmental neurotoxicity testing. Toxicology 2008, 249:243-250. 10.1016/j.tox.2008.05.014.
23. Hoffmann S., Kinsner-Ovaskainen A., Prieto P., Mangelsdorf I., Bieler C., Cole T. Acute oral toxicity: variability, reliability, relevance and interspecies comparison of rodent LD50 data from literature surveyed for the ACuteTox project. Regul. Toxicol. Pharmacol. 2010, 58:395-407. 10.1016/j.yrtph.2010.08.004.
24. Holownia A., Mroz R.M., Wielgat P., Skiepko A., Sitko E., Jakubow P., Kolodziejczyk A., Braszko J.J. Propofol protects rat astrigilas cells against tert-butyl hydroperoxide-induced cytotoxicity; the effect on histone and cAMP-response element-binding protein (CREB). Signaling 2009, 63-69.
25. Hu B., Weick J.P., Yu J., Ma L., Zhang X., Thomson J.A. Neural differentiation of human induced pluripotent stem cells follows developmental principles but with variable potency 2010, 1. 10.1073/pnas.0910012107.
26. Irons H.R., Cullen D.K., Shapiro N.P., Lambert N.a, Lee R.H., Laplaca M.C. Three-dimensional neural constructs: a novel platform for neurophysiological investigation. J. Neural Eng. 2008, 5:333-341. 10.1088/1741-2560/5/3/006.
27. Kim K., Lee S.-G., Kegelman T.P., Su Z.-Z., Das S.K., Dash R., Dasgupta S., Barral P.M., Hedvat M., Diaz P., Reed J.C., Stebbins J.L., Pellecchia M., Sarkar D., Fisher P.B. Role of excitatory amino acid transporter-2 (EAAT2) and glutamate in neurodegeneration: opportunities for developing novel therapeutics. J. Cell. Physiol. 2011, 226:2484-2493. 10.1002/jcp.22609.
28. Laurenza I., Pallocca G., Mennecozzi M., Scelfo B., Pamies D., Bal-Price A. A human pluripotent carcinoma stem cell-based model for in vitro developmental neurotoxicity testing: effects of methylmercury, lead and aluminum evaluated by gene expression studies. Int. J. Dev. Neurosci. 2013, 31:679-691. 10.1016/j.ijdevneu.2013.03.002.
29. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408. 10.1006/meth.2001.1262.
30. Lopachin, R.M., Gavin, T., 2012. Review molecular mechanism of acrylamide neurotoxicity: lessons learned from organic chemistry 1650-1657.
31. Materne E.-M., Ramme A.P., Terrasso A.P., Serra M., Alves P.M., Brito C., Sakharov D.A., Tonevitsky A.G., Lauster R., Marx U. A multi-organ chip co-culture of neurospheres and liver equivalents for long-term substance testing. J. Biotechnol. 2014, (submitted).
32. Michalczyk, K., Ziman, M., 2005. Nestin structure and predicted function in cellular cytoskeletal organisation 665-671.
33. Molofsky A.V., Krencik R., Krenick R., Ullian E.M., Ullian E., Tsai H., Deneen B., Richardson W.D., Barres B.a, Rowitch D.H. Astrocytes and disease: a neurodevelopmental perspective. Genes Dev. 2012, 26:891-907. 10.1101/gad.188326.112.
34. Moors M., Rockel T.D., Abel J., Cline J.E., Gassmann K., Schreiber T., Schuwald J., Weinmann N., Fritsche E. Human neurospheres as three-dimensional cellular systems for developmental neurotoxicity testing. Environ. Health Perspect. 2009, 117:1131-1138. 10.1289/ehp.0800207.
35. Mori H., Hara M. Cultured stem cells as tools for toxicological assays. J. Biosci. Bioeng. 2013, 116:647-652. 10.1016/j.jbiosc.2013.05.028.
36. Mundy W., Padilla S., Shafer T., Gilbert M., Breier J., Cowden J., Crofton K., Herr D., Jensen K., Raffaele K., Radio N., Schumacher K., Epa N.D.U.S., Toxicology C., Chapel N.C., Hill C., Ord N., Epa U.S., City K. Building a database of developmental neurotoxicants: evidence from human and animal studies. Toxicologist 2009, 108.
37. Ramilo O., Kinane B., McCracken G. Chloramphenicol neurotoxicity. Pediatr. Infect. Dis. J. 1988, 7:358.
38. Schwarz, J., 2007. Developmental perspectives on human midbrain-derived neural stem cells 13, 466-468.
39. Serra, M., Brito, C., Costa, E.M., Sousa, M.F.Q., Alves, P.M., 2009. Integrating human stem cell expansion and neuronal differentiation in bioreactors 14, 1-14. doi:10.1186/1472-6750-9-82.
40. Serra M., Brito C., Sousa M.F.Q., Jensen J., Tostões R., Clemente J., Strehl R., Hyllner J., Carrondo M.J.T., Alves P.M. Improving expansion of pluripotent human embryonic stem cells in perfused bioreactors through oxygen control. J. Biotechnol. 2010, 148:208-215. 10.1016/j.jbiotec.2010.06.015.
41. Serra, M., Leite, S.B., Brito, C., Carrondo, M.J.T., Alves, P.M., 2007. Novel culture strategy for human stem cell proliferation and neuronal differentiation 3566, 3557-3566. doi:10.1002/jnr.
42. Sofroniew, M. V, Vinters, H. V, 2010. Astrocytes: biology and pathology 7-35. doi:10.1007/s00401-009-0619-8.
43. Stern M., Gierse A., Tan S., Bicker G. Human Ntera2 cells as a predictive in vitro test system for developmental neurotoxicity. Arch. Toxicol. 2013, 10.1007/s00204-013-1098-1.
44. Tonge P.D., Andrews P.W. Retinoic acid directs neuronal differentiation of human pluripotent stem cell lines in a non-cell-autonomous manner. Differentiation 2010, 80:20-30. 10.1016/j.diff.2010.04.001.
45. Tralau T., Luch A. Drug-mediated toxicity: illuminating the bad in the test tube by means of cellular assays?. Trends Pharmacol. Sci. 2012, 1-12. 10.1016/j.tips.2012.03.015.
46. Trumpi, K., Egan, D.A., Vellinga, T.T., Rinkes, I.H. B., Kranenburg, O.W., 2014. High throughput toxicity assay for three-dimensional cell cultures, in: AACR Annual Meeting 2014; April 5-9, 2014; San Diego, CA.
47. Woehrling, E.K., Hill, E.J., Torr, E.E., Coleman, M.D., 2011. Single-cell ELISA and flow cytometry as methods for highlighting potential neuronal and astrocytic toxicant specificity 472-483. doi:10.1007/s12640-010-9202-2.
48. Zou J., Wang Y.-X., Dou F.-F., Lü H.-Z., Ma Z.-W., Lu P.-H., Xu X.-M. Glutamine synthetase down-regulation reduces astrocyte protection against glutamate excitotoxicity to neurons. Neurochem. Int. 2010, 56:577-584. 10.1016/j.neuint.2009.12.021.